Advertisement

Mycological Progress

, Volume 16, Issue 5, pp 535–552 | Cite as

Additions to Lindgomyces (Lindgomycetaceae, Pleosporales, Dothideomycetes), including two new species occurring on submerged wood from North Carolina, USA, with notes on secondary metabolite profiles

  • Huzefa A. Raja
  • Noemi D. Paguigan
  • Jacques Fournier
  • Nicholas H. Oberlies
Original Article

Abstract

Two new species of freshwater ascomycetes belonging to the genus Lindgomyces (Pleosporales, Dothideomycetes) are described and illustrated from submerged wood in North Carolina, USA. Lindgomyces carolinensis is characterized by immersed to erumpent ascomata, fissitunicate broadly cylindrical to clavate asci, and fusiform ascospores with acute ends surrounded by a large, fusiform gelatinous sheath. Lindgomyces cigarospora morphologically differs from L. carolinensis in that its ascospores are fusiform to cylindrical with rounded ends, without a large fusiform gelatinous sheath. These two new species nest in the family Lindgomycetaceae based on analyses of combined SSU and LSU rDNA sequence data. Phylogenetic analyses using ITS sequence data support the establishment of the new taxa as separate species within Lindgomyces. In addition to the new species, we report new ITS sequence data for L. cinctosporus and L. griseosporus from France, and L. ingoldianus from North Carolina, USA. We report a video exhibiting fissitunicate ascus dehiscence in L. carolinensis showing ascospore discharge and unraveling of the gelatinous sheath in real time. Chemical analysis of the organic extracts of L. carolinensis and L. cigarospora resulted in two known cyclodepsipeptides, Sch 378161 and Sch 217048. The in situ spatial mapping of these secondary metabolites on fungal cultures indicates the presence of both compounds on the surface of mycelia, as well as being exuded into the surrounding agar.

Keywords

Freshwater fungi Natural products chemistry Ribosomal genes Systematics 

Notes

Acknowledgements

We thank Dr. J.O. Falkinham, III of Virginia Polytechnic and State University for the antimicrobial testing and Dr. J. Burdette of the University of Illinois at Chicago for the cytotoxicity testing. We also thank Drs. V. Kertesz and G.J. Van Berkel of the Mass Spectrometry and Laser Spectroscopy Group, Chemical Sciences Division (Oak Ridge National Laboratory) for their guidance with the droplet-LMJ-SSP. We thank Dr. A. N Miller, Director of Illinois Natural History Fungarium for providing the ILLS accession numbers for holotype specimens.

Supplementary material

(MOV 5670 kb)

References

  1. Abdel-Aziz FA, Abdel-Wahab MA (2010) Lolia aquatica gen. et sp. nov. (Lindgomycetaceae, Pleosporales), a new coelomycete from freshwater habitats in Egypt. Mycotaxon 114:33–42. doi: 10.5248/114.33 CrossRefGoogle Scholar
  2. Ayers S, Graf TN, Adcock AF, Kroll DJ, Matthew S, Carcache de Blanco EJ, Shen Q, Swanson SM, Wani MC, Pearce CJ (2011) Resorcylic acid lactones with cytotoxic and NF-κB inhibitory activities and their structure–activity relationships. J Nat Prod 74:1126–1131. doi: 10.1021/np200062x CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ayers S, Ehrmann BM, Adcock AF, Kroll DJ, Carcache de Blanco EJ, Shen Q, Swanson SM, Falkinham JO, Wani MC, Mitchell SM, Pearce CJ (2012) Peptaibols from two unidentified fungi of the order Hypocreales with cytotoxic, antibiotic, and anthelmintic activities. J Pept Sci 18:500–510. doi: 10.1002/psc.2425 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Berbee ML (1996) Loculoascomycete origins and evolution of filamentous ascomycete morphology based on 18S rRNA gene sequence data. Mol Biol Evol 13(3):462–470CrossRefPubMedGoogle Scholar
  5. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefPubMedGoogle Scholar
  6. Chu M, Chan TM, Das P, Mierzwa R, Patel M, Puar M (2000) Structure of Sch 218157, a cyclodepsipeptide with neurokinin activity. J Antibiot 53:736–738CrossRefPubMedGoogle Scholar
  7. Crous PW, Wingfield MJ, Le Roux JJ, Richardson DM, Strasberg D, Shivas RG, Alvarado P, Edwards J, Moreno G, Sharma R (2015) Fungal Planet description sheets: 371–399. Persoonia 35:264–327. doi: 10.3767/003158515X690269 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi: 10.1038/nmeth.2109 CrossRefPubMedPubMedCentralGoogle Scholar
  9. de Gruyter J, Aveskamp MM, Woudenberg JH, Verkley GJ, Groenewald JZ, Crous PW (2009) Molecular phylogeny of Phoma and allied anamorph genera: towards a reclassification of the Phoma complex. Mycol Res 113:508–519. doi: 10.1016/j.mycres.2009.01.002 CrossRefPubMedGoogle Scholar
  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi: 10.1093/Nar/Gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  11. El-Elimat T, Figueroa M, Ehrmann BM, Cech NB, Pearce CJ, Oberlies NH (2013) High-resolution MS, MS/MS, and UV database of fungal secondary metabolites as a dereplication protocol for bioactive natural products. J Nat Prod 76:1709–1716. doi: 10.1021/np4004307 CrossRefPubMedGoogle Scholar
  12. El-Elimat T, Raja HA, Figueroa M, Falkinham JO III, Oberlies NH (2014a) Isochromenones, isobenzofuranone, and tetrahydronaphthalenes produced by Paraphoma radicina, a fungus isolated from a freshwater habitat. Phytochemistry 104:114–120. doi: 10.1016/j.phytochem.2014.04.006 CrossRefPubMedGoogle Scholar
  13. El-Elimat T, Raja HA, Day CS, Chen W-L, Swanson SM, Oberlies NH (2014b) Greensporones: resorcylic acid lactones from an aquatic Halenospora sp. J Nat Prod 77:2088–2098. doi: 10.1021/np500497r CrossRefPubMedPubMedCentralGoogle Scholar
  14. El-Elimat T, Raja HA, Day CS, McFeeters H, McFeeters RL, Oberlies NH (2017) α-Pyrone derivatives, tetra/hexahydroxanthones, and cyclodepsipeptides from two freshwater fungi. Bioorg Med Chem 25:795–804CrossRefPubMedGoogle Scholar
  15. Falkinham JO, Macri RV, Maisuria BB, Actis ML, Sugandhi EW, Williams AA, Snyder AV, Jackson FR, Poppe MA, Chen L, Ganesh K (2012) Antibacterial activities of dendritic amphiphiles against nontuberculous mycobacteria. Tuberculosis 92:173–181. doi: 10.1016/j.tube.2011.12.002 CrossRefPubMedGoogle Scholar
  16. Fallah PM, Shearer CA, Chen WD (1997) Ascovaginospora stellipala gen. et sp. nov. from sphagnum bogs. Mycologia 89:812–818CrossRefGoogle Scholar
  17. Felsenstein J (1980) Confidence intervals on phylogenies: an approach using bootstrap. Evolution 39:1792–1797Google Scholar
  18. Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11:481–487. doi: 10.1016/j.mib.2008.10.007 CrossRefPubMedGoogle Scholar
  19. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118CrossRefPubMedGoogle Scholar
  20. González-Medina M, Prieto-Martínez FD, Naveja JJ, Méndez-Lucio O, El-Elimat T, Pearce CJ, Oberlies NH, Figueroa M, Medina-Franco JL (2016) Chemoinformatic expedition of the chemical space of fungal products. Future Med Chem 8:1399–1412. doi: 10.4155/fmc-2016-0079 CrossRefPubMedGoogle Scholar
  21. Hegde VR, Puar MS, Chan TM, Dai P, Das PR, Patel M (1998) Sch 217048: a novel cyclodepsipeptide with neurokinin antagonist activity. J Org Chem 63:9584–9586CrossRefGoogle Scholar
  22. Hegde VR, Puar MS, Dai P, Pu H, Patel M, Anthes JC, Richard C, Terracciano J, Das PR, Gullo V (2001) A family of depsi-peptide fungal metabolites, as selective and competitive human tachykinin receptor (NK2) antagonists. Fermentation, isolation, physico-chemical properties, and biological activity. J Antibiot 54:125–135CrossRefGoogle Scholar
  23. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192CrossRefGoogle Scholar
  24. Hirayama K, Tanaka K, Raja HA, Miller AN, Shearer CA (2010) A molecular phylogenetic assessment of Massarina ingoldiana sensu lato. Mycologia 102:729–746. doi: 10.3852/09-230 CrossRefPubMedGoogle Scholar
  25. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  26. Huelsenbeck JP, Ronquist F (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical methods in molecular ecology. Springer, New YorkGoogle Scholar
  27. Hyde KD (1993) Tropical Australian freshwater fungi. VI*. Tiarosporella paludosa and Clohesyomyces aquaticus gen. et sp. nov. (Coelomycetes). Aust Syst Bot 6:169–173CrossRefGoogle Scholar
  28. Hyde KD, Jones EBG, Liu JK, Ariyawansa H, Boehm E, Boonmee S, Braun U, Chomnunti P, Crous PW, Dai DQ, Diederich P, Dissanayake A, Doilom M, Doveri F, Hongsanan S, Jayawardena R, Lawrey JD, Li YM, Liu YX, Lücking R, Monkai J, Muggia L, Nelsen MP, Pang KL, Phookamsak R, Senanayake IC, Shearer CA, Suetrong S, Tanaka K, Thambugala KM, Wijayawardene NN, Wikee S, Wu HX, Zhang Y, Aguirre-Hudson B, Alias SA, Aptroot A, Bahkali AH, Bezerra JL, Bhat DJ, Camporesi E, Chukeatirote E, Gueidan C, Hawksworth DL, Hirayama K, De Hoog S, Kang JC, Knudsen K, Li WJ, Li XH, Liu ZY, Mapook A, McKenzie EHC, Miller AN, Mortimer PE, Phillips AJL, Raja HA, Scheuer C, Schumm F, Taylor JE, Tian Q, Tibpromma S, Wanasinghe DN, Wang Y, Xu JC, Yacharoen S, Yan JY, Zhang M (2013) Families of Dothideomycetes. Fungal Divers 63:1–313. doi: 10.1007/S13225-013-0263-4 CrossRefGoogle Scholar
  29. Hyde KD, Hongsanan S, Jeewon R, Bhat DJ, McKenzie EH, Jones EG, Phookamsak R, Ariyawansa HA, Boonmee S, Zhao Q et al (2016) Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 80:1–270. doi: 10.1007/s13225-016-0373-x CrossRefGoogle Scholar
  30. Isaka M, Palasarn S, Komwijit S, Somrithipol S, Sommai S (2014) Pleosporin A, an antimalarial cyclodepsipeptide from an elephant dung fungus (BCC 7069). Tetrahedron Lett 55:469–471. doi: 10.1016/j.tetlet.2013.11.063 CrossRefGoogle Scholar
  31. Jones EG (2006) Form and function of fungal spore appendages. Mycoscience 47:167–183. doi: 10.1007/s10267-006-0295-7 CrossRefGoogle Scholar
  32. Kruys Å, Eriksson OE, Wedin M (2006) Phylogenetic relationships of coprophilous Pleosporales (Dothideomycetes, Ascomycota), and the classification of some bitunicate taxa of unknown position. Mycol Res 110:527–536. doi: 10.1016/j.mycres.2006.03.002 CrossRefPubMedGoogle Scholar
  33. Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA et al (2016) Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 78:1–237. doi: 10.1007/s13225-016-0366-9 CrossRefGoogle Scholar
  34. Liew EC, Aptroot A, Hyde KD (2000) Phylogenetic significance of the pseudoparaphyses in Loculoascomycete taxonomy. Mol Phylogenet Evol 16:392–402. doi: 10.1006/mpev.2000.0801 CrossRefPubMedGoogle Scholar
  35. Liu JK, Hyde KD, Jones EG, Ariyawansa HA, Bhat DJ, Boonmee S, Maharachchikumbura SS, McKenzie EH, Phookamsak R, Phukhamsakda C et al (2015) Fungal diversity notes 1–110: taxonomic and phylogenetic contributions to fungal species. Fungal Divers 72:1–197. doi: 10.1007/s13225-015-0324-y CrossRefGoogle Scholar
  36. LoBuglio KF, Berbee ML, Taylor JW (1996) Phylogenetic origins of the asexual mycorrhizal symbiont Cenococcum geophilum Fr. and other mycorrhizal fungi among the ascomycetes. Mol Phylogenet Evol 6:287–294CrossRefPubMedGoogle Scholar
  37. Lumbsch HT, Lindemuth R (2001) Major lineages of Dothideomycetes (Ascomycota) inferred from SSU and LSU rDNA sequences. Mycol Res 105:901–908CrossRefGoogle Scholar
  38. Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung GH, Lücking R, Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim YW, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91:1446–1480. doi: 10.3732/ajb.91.10.1446 CrossRefPubMedGoogle Scholar
  39. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for Inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 14 November 2010Google Scholar
  40. Paguigan ND, Raja HA, Day CS, Oberlies NH (2016) Acetophenone derivatives from a freshwater fungal isolate of recently described Lindgomyces madisonensis (G416). Phytochemistry 126:59–65. doi: 10.1016/j.phytochem.2016.03.007 CrossRefPubMedGoogle Scholar
  41. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi: 10.1080/10635150490522304 CrossRefPubMedGoogle Scholar
  42. Raja HA, Shearer CA (2008) Freshwater ascomycetes: new and noteworthy species from aquatic habitats in Florida. Mycologia 100:467–489. doi: 10.3852/07-167R CrossRefPubMedGoogle Scholar
  43. Raja HA, Schoch CL, Hustad VP, Shearer CA, Miller AN (2011a) Testing the phylogenetic utility of MCM7 in the Ascomycota. MycoKeys 1:63–94. doi: 10.3897/mycokeys.1.1966 CrossRefGoogle Scholar
  44. Raja HA, Tanaka K, Hirayama K, Miller AN, Shearer CA (2011b) Freshwater ascomycetes: two new species of Lindgomyces (Lindgomycetaceae, Pleosporales, Dothideomycetes) from Japan and USA. Mycologia 103:1421–1432. doi: 10.3852/11-077 CrossRefPubMedGoogle Scholar
  45. Raja HA, Oberlies NH, El-Elimat T, Miller AN, Zelski SE, Shearer CA (2013a) Lindgomyces angustiascus, (Lindgomycetaceae, Pleosporales, Dothideomycetes), a new lignicolous species from freshwater habitats in the USA. Mycoscience 54:353–361. doi: 10.1016/j.myc.2012.12.004 CrossRefGoogle Scholar
  46. Raja HA, Oberlies NH, Figueroa M, Tanaka K, Hirayama K, Hashimoto A, Miller AN, Zelski SE, Shearer CA (2013b) Freshwater ascomycetes: Minutisphaera (Dothideomycetes) revisited, including one new species from Japan. Mycologia 105:959–976. doi: 10.3852/12-313 CrossRefPubMedGoogle Scholar
  47. Raja HA, El-Elimat T, Oberlies NH, Shearer CA, Miller AN, Tanaka K, Hashimoto A, Fournier J (2015) Minutisphaerales (Dothideomycetes, Ascomycota): a new order of freshwater ascomycetes including a new family, Minutisphaeraceae, and two new species from North Carolina, USA. Mycologia 107:845–862. doi: 10.3852/15-013 CrossRefPubMedGoogle Scholar
  48. Rehner SA, Samuels GJ (1995) Molecular systematics of the hypocreales: a teleomorph gene phylogeny and the status of their anamorphs. Can J Bot 73:S816–S823CrossRefGoogle Scholar
  49. Rohlfs M (2015) Fungal secondary metabolite dynamics in fungus–grazer interactions: novel insights and unanswered questions. Front Microbiol 5:788. doi: 10.3389/fmicb.2014.00788 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Rossman AY, Farr DF, Castlebury LA, Shoemaker R, Mengistu A (2002) Setomelanomma holmii (Pleosporales, Phaeosphaeriaceae) on living spruce twigs in Europe and North America. Can J Bot 80:1209–1215. doi: 10.1139/b02-111 CrossRefGoogle Scholar
  51. Schoch CL, Kohlmeyer J, Volkmann-Kohlmeyer B, Tsui CK, Spatafora JW (2006a) The halotolerant fungus Glomerobolus gelineus is a member of the Ostropales. Mycol Res 110:257–263. doi: 10.1016/j.mycres.2005.10.001 CrossRefPubMedGoogle Scholar
  52. Schoch CL, Shoemaker RA, Seifert KA, Hambleton S, Spatafora JW, Crous PW (2006b) A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98:1041–1052CrossRefPubMedGoogle Scholar
  53. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W; Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246. doi: 10.1073/Pnas.1117018109 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Shearer CA (1993) The freshwater Ascomycetes. Nova Hedwigia 56(1–2):1–33Google Scholar
  55. Shearer CA, Hyde KD (1997) Massarina ingoldiana, a new ascomycete from freshwater habitats. Mycologia 89:114–119CrossRefGoogle Scholar
  56. Shearer CA, Raja HA (2016) Freshwater Ascomycetes and their anamorphs. Accessed 1 Aug 2016Google Scholar
  57. Shearer CA, Langsam DM, Longcore JE (2004) Fungi in freshwater habitats. In: Mueller GM, Bills GF, Foster MS (eds) Measuring and monitoring biological diversity: standard methods for Fungi. Smithsonian Institution Press, Washington, DC, pp 513–531Google Scholar
  58. Shearer CA, Raja HA, Miller AN, Nelson P, Tanaka K, Hirayama K, Marvanová L, Hyde KD, Zhang Y (2009) The molecular phylogeny of freshwater Dothideomycetes. Stud Mycol 64:145–153. doi: 10.3114/Sim.2009.64.08 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sica VP, Raja HA, El-Elimat T, Kertesz V, Van Berkel GJ, Pearce CJ, Oberlies NH (2015) Dereplicating and spatial mapping of secondary metabolites from fungal cultures in situ. J Nat Prod 78:1926–1936. doi: 10.1021/acs.jnatprod.5b00268 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sica VP, Rees ER, Tchegnon E, Bardsley RH, Raja HA, Oberlies NH (2016) Spatial and temporal profiling of griseofulvin production in Xylaria cubensis using mass spectrometry mapping. Front Microbiol 7(e1002700):544. doi: 10.3389/fmicb.2016.00544 PubMedPubMedCentralGoogle Scholar
  61. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi: 10.1093/Bioinformatics/Btl446 CrossRefPubMedGoogle Scholar
  62. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  63. Tsang C-C, Chan JF, Trendell-Smith NJ, Ngan AH, Ling IW, Lau SK, Woo PC (2014) Subcutaneous phaeohyphomycosis in a patient with IgG4-related sclerosing disease caused by a novel ascomycete, Hongkongmyces pedis gen. et sp. nov.: first report of human infection associated with the family Lindgomycetaceae. Med Mycol 52:736–747. doi: 10.1093/mmy/myu043 CrossRefPubMedGoogle Scholar
  64. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246CrossRefPubMedPubMedCentralGoogle Scholar
  65. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and application. Academic Press, San Diego, pp 315–322Google Scholar
  66. Winka K (2000) Phylogenetic relationships within the Ascomycota based on 18S rDNA sequences. Doctoral dissertation, Umeå University, UmeåGoogle Scholar
  67. Zhang Y, Jeewon R, Fournier J, Hyde KD (2008) Multi-gene phylogeny and morphotaxonomy of Amniculicola lignicola: a novel freshwater fungus from France and its relationships to the Pleosporales. Mycol Res 112:1186–1194. doi: 10.1016/j.mycres.2008.04.004 CrossRefPubMedGoogle Scholar
  68. Zhang Y, Wang HK, Fournier J, Crous PW, Jeewon R, Pointing SB, Hyde KD (2009a) Towards a phylogenetic clarification of Lophiostoma/Massarina and morphologically similar genera in the Pleosporales. Fungal Divers 38:225–251Google Scholar
  69. Zhang Y, Schoch CL, Fournier J, Crous PW, De Gruyter J, Woudenberg JH, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD (2009b) Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 64:85–102. doi: 10.3114/sim.2009.64.04 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zhang H, Hyde KD, Mckenzie EH, Bahkali AH, Zhou D (2012a) Sequence data reveals phylogenetic affinities of Acrocalymma aquatica sp. nov., Aquasubmersa mircensis gen. et sp. nov. and Clohesyomyces aquaticus (freshwater coelomycetes). Cryptogam Mycol 33:333–346. doi: 10.7872/crym.v33.iss3.2012.333 CrossRefGoogle Scholar
  71. Zhang Y, Crous PW, Schoch CL, Hyde KD (2012b) Pleosporales. Fungal Divers 53:1–221. doi: 10.1007/s13225-011-0117-x CrossRefPubMedGoogle Scholar
  72. Zhang Y, Zhang X, Fournier J, Chen J, Hyde KD (2014) Lindgomyces griseosporus, a new aquatic ascomycete from Europe including new records. Mycoscience 55:43–48. doi: 10.1016/j.myc.2013.05.003 CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Huzefa A. Raja
    • 1
  • Noemi D. Paguigan
    • 1
  • Jacques Fournier
    • 2
  • Nicholas H. Oberlies
    • 1
  1. 1.Department of Chemistry and BiochemistryUniversity of North Carolina at GreensboroGreensboroUSA
  2. 2.Las MurosRimontFrance

Personalised recommendations